Mitogen- and stress-activated protein kinase 1 modulates photic entrainment of the suprachiasmatic circadian clock

European Journal of Neuroscience

Volumn 37, Issue 1, 2013, Pages 130-140

  Cao, Ruifeng ^a,d   Butcher, Greg Q ^b   Karelina, Kate ^a   Arthur, J Simon ^c   Obrietan, Karl ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b CENTENARY COLLEGE OF LOUISIANA   (United States)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

CREB; ERK; Light; Mitogen activated protein kinase; Mouse; Suprachiasmatic nucleus

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN A; MITOGEN ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ELECTRIC ACTIVITY; ENZYME ACTIVITY; EVOKED RESPONSE; GENE EXPRESSION; HISTONE PHOSPHORYLATION; INTRACELLULAR SIGNALING; LIGHT; LIGHT DARK CYCLE; LOCOMOTION; MALE; MOLECULAR BIOLOGY; MOUSE; MSK1 GENE; NONHUMAN; PERIOD1 GENE; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SUPRACHIASMATIC NUCLEUS;

ANIMALS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HISTONES; JET LAG SYNDROME; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; PERIOD CIRCADIAN PROTEINS; PHOSPHORYLATION; PHOTIC STIMULATION; PHOTOPERIOD; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SUPRACHIASMATIC NUCLEUS; TRANSCRIPTION, GENETIC;

EID: 84872127327     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12028     Document Type: Article

References (67)

1. Abrahamson, E.E. & Moore, R.Y. (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res., 916, 172-191.
2. Adams, J.P. & Sweatt, J.D. (2002) Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu. Rev. Pharmacol. Toxicol., 42, 135-163.
3. Ait-Si-Ali, S., Polesskaya, A., Filleur, S., Ferreira, R., Duquet, A., Robin, P., Vervish, A., Trouche, D., Cabon, F. & Harel-Bellan, A. (2000) CBP/p300 histone acetyl-transferase activity is important for the G1/S transition. Oncogene, 19, 2430-2437.
4. Akashi, M., Hayasaka, N., Yamazaki, S. & Node, K. (2008) Mitogen-activated protein kinase is a functional component of the autonomous circadian system in the suprachiasmatic nucleus. J. Neurosci., 28, 4619-4623.
5. Akiyama, M., Kouzu, Y., Takahashi, S., Wakamatsu, H., Moriya, T., Maetani, M., Watanabe, S., Tei, H., Sakaki, Y. & Shibata, S. (1999) Inhibition of light- or glutamate-induced mPer1 expression represses the phase shifts into the mouse circadian locomotor and suprachiasmatic firing rhythms. J. Neurosci., 19, 1115-1121.
6. Albrecht, U., Sun, Z.S., Eichele, G. & Lee, C.C. (1997) A differential response of two putative mammalian circadian regulators, mper1 and mper2, to light. Cell, 91, 1055-1064.
7. Albrecht, U., Zheng, B., Larkin, D., Sun, Z.S. & Lee, C.C. (2001) MPer1 and mper2 are essential for normal resetting of the circadian clock. J. Biol. Rhythms, 16, 100-104.
8. Anjum, R. & Blenis, J. (2008) The RSK family of kinases: emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol., 9, 747-758.
9. Arthur, J.S. (2008) MSK activation and physiological roles. Front. Biosci., 13, 5866-5879.
10. Arthur, J.S. & Cohen, P. (2000) MSK1 is required for CREB phosphorylation in response to mitogens in mouse embryonic stem cells. FEBS Lett., 482, 44-48.
11. Arthur, J.S., Fong, A.L., Dwyer, J.M., Davare, M., Reese, E., Obrietan, K. & Impey, S. (2004) Mitogen- and stress-activated protein kinase 1 mediates cAMP response element-binding protein phosphorylation and activation by neurotrophins. J. Neurosci., 24, 4324-4332.
12. Aschoff, J. (1965) Response curves in circadian periodicity. In Aschoff, J. (Ed.), Circadian Clocks. North-Holland, Amsterdam, pp. 95-111.
13. Brami-Cherrier, K., Valjent, E., Hervé, D., Darragh, J., Corvol, J.C., Pages, C., Arthur, S.J., Girault, J.A. & Caboche, J. (2005) Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J. Neurosci., 25, 11444-11454.
14. Butcher, G., Dziema, H., Collamore, M., Burgoon, P.W. & Obrietan, K. (2002) The p42/44 mitogen-activated protein kinase pathway couples photic input to circadian clock entrainment. J. Biol. Chem., 277, 29519-29525.
15. Butcher, G., Lee, B., Cheng, H.Y. & Obrietan, K. (2005) Light stimulates MSK1 activation in the suprachiasmatic nucleus via a PACAP-ERK/MAP kinase-dependent mechanism. J. Neurosci., 25, 5305-5313.
16. Butcher, G.Q., Lee, B., Hsieh, F. & Obrietan, K. (2004) Light- and clock-dependent regulation of ribosomal S6 kinase activity in the suprachiasmatic nucleus. Eur. J. Neurosci., 19, 907-915.
17. Cao, R., Lee, B., Cho, H.Y., Saklayen, S. & Obrietan, K. (2008) Photic regulation of the mTOR signaling pathway in the suprachiasmatic circadian clock. Mol. Cell. Neurosci., 38, 312-324.
18. Cao, R., Li, A., Cho, H.Y., Lee, B. & Obrietan, K. (2010) Mammalian target of rapamycin signaling modulates photic entrainment of the suprachiasmatic circadian clock. J. Neurosci., 30, 6302-6314.
19. Cao, R., Anderson, F.E., Jung, Y.J., Dziema, H. & Obrietan, K. (2011) Circadian regulation of mammalian target of rapamycin signaling in the mouse suprachiasmatic nucleus. Neuroscience, 181, 79-88.
20. Cheng, H., Dziema, H., Papp, J., Mathur, D.P., Koletar, M., Ralph, M.R., Penninger, J.M. & Obrietan, K. (2006) The molecular gatekeeper Dexras1 sculpts the photic responsiveness of the mammalian circadian clock. J. Neurosci., 26, 12984-12995.
21. Cheng, H.Y., Alvarez-Saavedra, M., Dziema, H., Choi, Y.S., Li, A. & Obrietan, K. (2009) Segregation of expression of mPeriod gene homologs in neurons and glia: possible divergent roles of mPeriod1 and mPeriod2 in the brain. Hum. Mol. Genet., 18, 3110-3124.
22. Clayton, A.L. & Mahadevan, L.C. (2003) MAP kinase-mediated phosphoacetylation of histone H3 and inducible gene regulation. FEBS Lett., 546, 51-58.
23. Coogan, A. & Piggins, H.D. (2003) Circadian and photic regulation of phosphorylation of ERK1/2 and Elk-1 in the suprachiasmatic nuclei of the Syrian hamster. J. Neurosci., 23, 3085-3093.
24. Crosio, C., Cermakian, N., Allis, C.D. & Sassone-Corsi, P. (2000) Light induces chromatin modification in cells of the mammalian circadian clock. Nat. Neurosci., 3, 1241-1247.
25. Crosio, C., Heitz, E., Allis, C.D., Borrelli, E. & Sassone-Corsi, P. (2003) Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J. Cell Sci., 116, 4905-4914.
26. Daan, S. & Pittendrigh, C.S. (1976) A functional analysis of circadian pacemakers in noctural rodents, II The variability of phase response curves. J. Comp. Physiol., 106, 253-266.
27. Deak, M., Clifton, A.D., Lucocq, L.M. & Alessi, D.R. (1998) Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J., 17, 4426-4441.
28. Ding, J., Faiman, L.E., Hurst, W.J., Kuriashkina, L.R. & Gillette, M.U. (1997) Resetting the biological clock: mediation of nocturnal CREB phosphorylation via light, glutamate, and nitric oxide. J. Neurosci., 17, 667-675.
29. Drobic, B., Pérez-Cadahía, B., Yu, J., Kung, S.K. & Davie, J.R. (2010) Promoter chromatin remodeling of immediate-early genes is mediated through H3 phosphorylation at either serine 28 or 10 by the MSK1 multi-protein complex. Nucleic Acids Res., 38, 3196-3208.
30. Dziema, H., Oatis, B., Butcher, G.Q., Yates, R., Hoyt, K.R. & Obrietan, K. (2003) The ERK/MAP kinase pathway couples light to immediate-early gene expression in the suprachiasmatic nucleus. Eur. J. Neurosci., 17, 1617-1627.
31. Frödin, M. & Gammeltoft, S. (1999) Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol. Cell. Endocrinol., 151, 65-77.
32. Ginty, D., Kornhauser, J.M., Thompson, M.A., Bading, H., Mayo, K.E., Takahashi, J.S. & Greenberg, M.E. (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science, 260, 238-241.
33. Golombek, D. & Ralph, M.R. (1995) Circadian responses to light: the calmodulin connection. Neurosci. Lett., 192, 101-104.
34. Golombek, D. & Rosenstein, R.E. (2010) Physiology of circadian entrainment. Physiol. Rev., 90, 1063-1102.
35. Gutièrrez-Mecinas, M., Trollope, A.F., Collins, A., Morfett, H., Hesketh, S.A., Kersanté, F. & Reul, J.M. (2011) Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc. Natl. Acad. Sci., 108, 13806-13811.
36. Hale, M.W., Hay-Schmidt, A., Mikkelsen, J.D., Poulsen, B., Shekhar, A. & Lowry, C.A. (2008) Exposure to an open-field arena increases c-Fos expression in a distributed anxiety-related system projecting to the basolateral amygdaloid complex. Neuroscience, 155, 659-672.
37. Korzus, E., Torchia, J., Rose, D.W., Xu, L., Kurokawa, R., McInerney, E.M., Mullen, T.M., Glass, C.K. & Rosenfeld, M.G. (1998) Transcription factor-specific requirements for coactivators and their acetyltransferase functions. Science, 279, 703-707.
38. Lee, B., Li, A., Hansen, K.F., Cao, R., Yoon, J.H. & Obrietan, K. (2010) CREB influences timing and entrainment of the SCN circadian clock. J. Biol. Rhythms, 25, 410-420.
39. Liu, B., Willette-Brown, J., Liu, S., Chen, X., Fischer, S.M. & Hu, Y. (2011) IKKα represses a network of inflammation and proliferation pathways and elevates c-Myc antagonists and differentiation in a dose-dependent manner in the skin. Cell Death Differ., 18, 1854-1864.
40. Lowrey, P.L. & Takahashi, J.S. (2011) Genetics of circadian rhythms in mammalian model organisms. Adv. Genet., 74, 231-247.
41. Lucibello, F.C., Ehlert, F. & Müller, R. (1991) Multiple interdependent regulatory sites in the mouse c-fos promoter determine basal level transcription: cell type-specific effects. Nucleic Acids Res., 19, 3583-3591.
42. McCoy, C.E., Campbell, D.G., Deak, M., Bloomberg, G.B. & Arthur, J.S. (2005) MSK1 activity is controlled by multiple phosphorylation sites. Biochem. J., 387, 507-517.
43. Meijer, J.H. & Schwartz, W.J. (2003) In search of the pathways for light-induced pacemaker resetting in the suprachiasmatic nucleus. J. Biol. Rhythms, 18, 235-249.
44. Obrietan, K., Impey, S. & Storm, D.R. (1998) Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nat. Neurosci., 1, 693-700.
45. Obrietan, K., Impey, S., Smith, D., Athos, J. & Storm, D.R. (1999) Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J. Biol. Chem., 274, 17748-17756.
46. -/- mutant mice. Genes Dev., 17, 1366-1379.
47. Pizzio, G.A., Hainich, E.C., Plano, S.A., Ralph, M.R. & Golombek, D.A. (2005) Nerve growth factor-induced circadian phase shifts and MAP kinase activation in the hamster suprachiasmatic nuclei. Eur. J. Neurosci., 22, 665-671.
48. Raman, M., Chen, W. & Cobb, M.H. (2007) Differential regulation and properties of MAPKs. Oncogene, 26, 3100-3112.
49. Reppert, S. & Weaver, D.R. (2002) Coordination of circadian timing in mammals. Nature, 418, 935-941.
50. Sakamoto, K., Karelina, K. & Obrietan, K. (2011) CREB: a multifaceted regulator of neuronal plasticity and protection. J. Neurochem., 116, 1-9.
51. Sands, W.A. & Palmer, T.M. (2008) Regulating gene transcription in response to cyclic AMP elevation. Cell. Signal., 20, 460-466.
52. Schurov, I.L., McNulty, S., Best, J.D., Sloper, P.J. & Hastings, M.H. (1999) Glutamatergic induction of CREB phosphorylation and Fos expression in primary cultures of the suprachiasmatic hypothalamus in vitro is mediated by co-ordinate activity of NMDA and non-NMDA receptors. J. Neuroendocrinol., 11, 43-51.
53. Schurov, I.L., Hepworth, T.J. & Hastings, M.H. (2002) Dopaminergic signalling in the rodent neonatal suprachiasmatic nucleus identifies a role for protein kinase A and mitogen-activated protein kinase in circadian entrainment. Eur. J. Neurosci., 15, 223-232.
54. Shigeyoshi, Y., Taguchi, K., Yamamoto, S., Takekida, S., Yan, L., Tei, H., Moriya, T., Shibata, S., Loros, J.J., Dunlap, J.C. & Okamura, H. (1997) Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell, 91, 1043-1053.
55. Soloaga, A., Thomson, S., Wiggin, G.R., Rampersaud, N., Dyson, M.H., Hazzalin, C.A., Mahadevan, L.C. & Arthur, J.S. (2003) MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14. EMBO J., 22, 2788-2797.
56. Stratford, J.M. & Finger, T.E. (2011) Central representational postingestive chemosensory cues in mice that lack the ability to taste. J. Neurosci., 31, 9101-9110.
57. Thomson, S., Clayton, A.L., Hazzalin, C.A., Rose, S., Barratt, M.J. & Mahadevan, L.C. (1999) The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J., 18, 4779-4793.
58. 2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the suprachiasmatic nucleus circadian clock. J. Biol. Chem., 278, 718-723.
59. Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M. & Sassone-Corsi, P. (2002) Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl. Acad. Sci., 99, 7728-7733.
60. Vermeulen, L., Vanden Berghe, W., Beck, I.M., De Bosscher, K. & Haegeman, G. (2009) The versatile role of MSKs in transcriptional regulation. Trends Biochem. Sci., 34, 311-318.
61. Vicent, G.P., Ballaré, C., Nacht, A.S., Clausell, J., Subtil-Rodríguez, A., Quiles, I., Jordan, A. & Beato, M. (2006) Induction of progesterone target genes requires activation of Erk and Msk kinases and phosphorylation of histone H3. Mol. Cell, 24, 367-381.
62. Viktorin, G., Riebli, N., Popkova, A., Giangrande, A. & Reichert, H. (2011) Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Dev. Biol., 353, 553-565.
63. Wakamatsu, H., Takahashi, S., Moriya, T., Inouye, S.T., Okamura, H., Akiyama, M. & Shibata, S. (2001) Additive effect of mPer1 and mPer2 antisense oligonucleotides on light-induced phase shift. NeuroReport, 12, 121-131.
64. Wiggin, G., Soloaga, A., Foster, J.M., Murray-Tait, V., Cohen, P. & Arthur, J.S. (2002) MSK1 and MSK2 are required for the mitogen- and stress-induced phosphorylation of CREB and ATF1 in fibroblasts. Mol. Cell. Biol., 22, 2871-2881.
65. Xia, Z., Dudek, H., Miranti, C.K. & Greenberg, M.E. (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci., 16, 5425-5436.
66. Xing, J., Ginty, D.D. & Greenberg, M.E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science, 273, 959-963.
67. Yuan, L.W. & Gambee, J.E. (2001) Histone acetylation by p300 is involved in CREB-mediated transcription on chromatin. Biochim. Biophys. Acta, 1541, 161-169.